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UNIVERSITY of CALIFORNIA, SAN DIEGO Evidence of Positive UNIVERSITY OF CALIFORNIA, SAN DIEGO Evidence of positive selection in the mitochondrial cytochrome B gene of cetaceans A Thesis submitted in partial satisfaction of the requirements for the degree Master of Science in Biology by Sarah Matsuye Urata Committee in charge: Professor Phillip A. Morin, Chair Professor David S. Woodruff, Co-Chair Professor Eric E. Allen 2014 The Thesis of Sarah Matsuye Urata is approved and it is acceptable in quality and form for publication on microfilm and electronically: Co-Chair Chair University of California, San Diego 2014 iii TABLE OF CONTENTS Signature Page ............................................................................................................... iii Table of Contents .......................................................................................................... iv List of Figures ................................................................................................................. v List of Tables ................................................................................................................. vi Abstract of the Thesis ................................................................................................... vii Introduction .................................................................................................................... 1 Methods .......................................................................................................................... 6 Results and Discussion ................................................................................................. 11 Conclusions .................................................................................................................. 23 Appendix ...................................................................................................................... 26 References .................................................................................................................... 28 iv LIST OF FIGURES Figure 1: Phylogenetic tree inferred using MrBayes. Tip labels consist of accession number and species. Nodes are labeled with the posterior probability. ........... 13 Figure 2: Graphical summary of cytochrome b regions that were identified as being under positive selection (magnitude categories 6-8 with a z-score of 3.09 or greater) by TreeSAAP. Each series represents a different property that is suggested to be undergoing this selection. ....................................................... 15 Figure 3: Points represent the number of radical amino acid property changes identified at residue numbers with a p ≤ 0.001 across all lineages represented in the study (refer to Figure 1 for phylogeny). ................................................. 19 v LIST OF TABLES Table 1: GenBank Accession Numbers for mitogenome sequences used in this study (66 complete mitogenome sequences from 46 species; this includes H. amphibius as an outgroup) .................................................................................. 8 Table 2: Summary of alignment gaps removed for Codeml and PAML analysis. Within the ND1 gene, 4 bases were removed due to a one base difference in AJ554060 (P. blainvillei, a river dolphin) ........................................................ 12 Table 3: Summary of cytochrome b secondary structure. Codon positions based on Protein database (PDB), ID: 1PPJ, Chain C (Huang, et al. 2005). ................... 17 Table 4: Codon sites at which the change within the branch is specific only to that respective branch .............................................................................................. 21 Table 5: Physicochemical amino acid properties (31) used for selection analysis in TreeSAAP ......................................................................................................... 26 Table 6: Site Models tested using codeml in the PAML package; p is the number of free parameters that are estimated in each model ............................................. 27 vi ABSTRACT OF THE THESIS Evidence of positive selection in the mitochondrial cytochrome B gene of cetaceans by Sarah Matsuye Urata Master of Science in Biology University of California, San Diego, 2014 Professor Phillip A. Morin, Chair Professor David S. Woodruff, Co-Chair Mitochondrial genomes (mitogenomes) code for, in part, the enzymes involved in the creation of energy for cellular function. Altering these highly conserved genes even slightly can have a biochemical impact on this pathway. Analyzing the mitogenome for positive selection using models that take biochemically significant changes into account can identify adaptive alterations presumably under selection due vii to energetic costs that vary across lineages due to physiological divergence, environmental factors, or ecological drivers. This study was conducted on the mitochondrial cytochrome B (CYTB) gene of 45 cetacean species. Using TreeSAAP, I identified evidence of positive selection based on five physicochemical properties acting on several of the transmembrane helical regions of CYTB. In addition to these broad regional findings, 88 codon sites were identified to have undergone radical and significant changes. Further computational analysis will be necessary in order to better resolve which codons are undergoing adaptive changes. This study was not able to conclusively identify any singular metabolic driver for amino acid alterations among lineages. viii INTRODUCTION Genes within the mitochondrial genome (mitogenome) code for proteins critical for oxidative phosphorylation, the pathway involved in producing adenosine triphosphate (ATP), which is ultimately used to energetically carry out many other reactions within the cell. The mechanism by which this is accomplished is through a serious of reducing and oxidizing (redox) reactions carried out by enzymes embedded within the mitochondrial inner membrane (Saraste 1999). Alterations in these genes may have functional impacts on the enzymes’ ability to perform these reactions. Analyzing the mitogenome for positive selection, based on models that take into account the biochemical significance of the genetic variation, can identify adaptive changes to this metabolic pathway resulting from various energetic costs experienced by individuals due to evolutionary divergence, environmental factors, or ecological drivers. Nucleotide variants that resulted in amino acid changes were previously identified in the mitochondrial cytochrome B (CYTB) gene of several species (McClellan, et al. 2005; Foote, et al. 2011). Cytochrome B is part of complex three within the electron transport chain. Complex three’s main function is within the Q- cycle in which an electron carrier coenzyme ubiquinol is oxidized to ubiquinone (Cramer, et al. 2011). Looking at the artiodactyls compared to cetaceans, the transition from a land environment to an aquatic habitat likely incurred a shift in metabolic pressure on organisms and therefore could be the driver for the observed differences in the cyt b genes (McClellan, et al. 2005). 1 2 Sites in the CYTB gene have also appeared to be under positive selection in killer whales; these amino acid changes resulted in an alteration of polarity in the protein residues (Foote, et al. 2011). It has been hypothesized that these changes are under positive selection due to varying metabolic pressures on differing types of killer whales, which have previously been classified into ecotypes (Pitman and Ensor 2003; LeDuc, et al. 2008). When there is a nucleotide change in the DNA sequence, this change can be classified as either a synonymous change in which the resulting amino acid is the same or a non-synonymous change in which the resulting amino acid is different. Non- synonymous changes are the basis for protein evolution, subject to natural selection. Positive selection at the molecular level has been identified by a variety of methods. A simple method for detecting the effects of positive selection on a protein sequence is the dN/dS ratio (ω = dN/dS) (Li 1993). Omega (ω) is the ratio of the non- synonymous substitution rate (dN) to the synonymous substitution rate (dS). A ratio of one implies selective neutrality. A ratio of less than one implies that purifying selection is acting upon the gene or sequence of interest. If this ratio is greater than one, this signifies positive selection (Yang and Nielsen 2000). This method of detection of positive selection is useful but more difficult to interpret when dealing with well conserved sequences. When a sequence is highly conserved, even one amino acid change from a non-synonymous substitution can have a significant impact on the protein. Newer models that test for positive selection have been developed in light of this. These models take into consideration the base/codon frequency bias, transition/transversion rate bias (Yang and Nielsen 2000), and/or the 3 physicochemical properties of amino acids (Woolley, et al. 2003). These models improve the search for identifying positive selection within conserved sequences because they can allow selectively neutral evolution to be more complex than simply random mutations and they test for biochemical (protein-level) significance as a driving force for positive selection. Mitogenomes and single nucleotide polymorphisms (SNPs) have been predominantly used in cetacean genetics as evidence for phylogenies and/or population structure (e.g., Morin, et al. 2009; Morin, et al. 2010; Duchene, et al. 2011). These studies typically
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